Proceratophrys belzebul

Carrasco-Medina, Andres Santiago, Ernetti, Julia R., Botelho, Lucas Machado, Muscat, Edelcio & Toledo, L. Felipe, 2024, Description and natural history notes of the tadpole of Proceratophrys belzebul (Anura: Odontophrynidae), Zootaxa 5474 (3), pp. 292-296 : 292-295

Tadpoles

were collected at Parque Estadual da Serra do Mar (Núcleo Santa Virgínia), municipality of Natividade da Serra , state of São Paulo, Brazil, in a locality known as “Trilha do campinho” (23º52’67”S, 45º33’14”W, 855 m above sea level). The individuals were collected on 3 March 2022, from a small stream in a calm section with sandy bottom by active method using a dip net. Twelve tadpoles were analyzed and staged following Gosner (1960): St. 35 (n = 3), St. 37 (n = 1), St. 39 (n = 3), and St. 41 (n = 5). Measurements were registered using a stereoscopic microscope (Leica S 9). Tadpoles at St. 35–39 (n = 7) were analyzed to characterize the oral structures of the species. Photographs were taken with a ZEISS Discovery V 20 stereoscope with an AxioCam MRc5 camera. Nomenclature and measurements follows Haas & Das (2011). Sampling permit were provided by the Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio) (SISBio #27745-26) and the Instituto Florestal do Estado de São Paulo (IF #004767/2020-42). Tadpoles were euthanized using 5% xylocaine, preserved in 10% formalin, and deposited in the Museu de Diversidade Biológica (MDBio) at the Universidade Estadual de Campinas, Campinas, São Paulo, Brazil (ZUEC-AMP 25335 – tadpole lot).

External morphology (Stages 35–41). Body elliptical in dorsal view and depressed in lateral view ( Fig. 1A ). Body length about 42% (39–61%) of total length ( Table 1 ). Snout rounded both in dorsal and lateral view, with nostrils elliptical and positioned dorsally ( Fig. 1B,C ). Eyes located dorsolaterally ( Fig. 1A–C ). Spiracle free, sinistral, and tubular-shaped, with posterodorsal orientation and with internal wall longer than the external ( Fig. 1D ). Vent tube medial and attached to the ventral fin. The dorsal and ventral fins originate slightly anterior to the body-tail junction, with the dorsal fin being slightly higher than the ventral one. The tail musculature does not extend all the way to the end of the fin. Oral disc ventral, emarginate, and bordered by a single row of alternate, conical marginal papillae ( Fig. 1E ). Labial tooth row formula (LTRF) 2/3(1), with A2> A1 and P1> P2> P 3 in all tadpoles.

In life the tadpole shows a reddish-brown body adorned with copper-colored spots extending from the dorsal to the lateral regions. Towards the lower lateral area, the body becomes increasingly transparent, allowing observation of the digestive tract. Eyes feature a light brown iris, marked by darker brown spots; closer to the pupil, the iris takes on a coppery hue, while the pupil remains distinctly black. Both the tail and fins exhibit a predominantly transparent appearance, adorned with sporadic brown markings. In formalin, the walls of the body and tail are transparent, revealing small brown melanophores that can be observed in the dorsal region and dispersed across the tail.

Natural history. The tadpoles of P. belzebul were observed in an area characterized by dense forest with little sunlight, in a small rocky stream surrounding flooded areas. They were found in lentic portions of the stream with a fine sandy bottom and decomposing leaves, occupying the same habitat as tadpoles of Hylodes sp. Adults inhabit the leaf litter of forest, obligate in primary and secondary rainforest within the Atlantic Forest biome.

In general, tadpoles of the species in the P. appendiculata group are typically found in slow-moving sections of streams, where they can be observed near the sandy substrate ( Dias et al. 2013a). These tadpoles are classified as benthic and exhibit cryptic behavior by blending in with the sand, as observed for P. belzebul tadpoles. This would minimize predation risk, as the tadpoles are challenging to distinguish when nestled in the sandy environment ( Peixoto et al. 1981; Fatorelli et al. 2010; Provete et al. 2013; Dias et al. 2014).

Tadpoles of the P. appendiculata species complex exhibit a conserved body shape, as well as other species of the genus (see Provete et al. 2013). A striking difference observed in P. belzebul with the tadpoles already described in the group is the presence of a spiracle with a free internal wall in the outermost region, which is larger than the external wall. This spiracle characteristic had only previously been reported in P. melanopogon tadpoles ( Provete et al. 2013). The oral papillae remain consistent with those of other genera, comprising a single row of conical papillae ( Provete et al. 2013; Dias et al. 2014). The tooth rows in P. belzebul individuals were difficult to observe as they did not show the typical keratinization normally observed in other tadpoles of the genus Proceratophrys ( Vieira et al. 2007; Fatorelli et al. 2010; Provete et al. 2013; Dias et al. 2014). Nevertheless, we confirm a LTRF 2/3(1), suggested as a putative synapomorphy for the P. appendiculata clade also integrated by P. izecksohni , P. tupinamba , and P. appendiculata ( Dias et al. 2014) . The observed absence of keratinization in the oral region is likely caused by Batrachochytrium dendrobatidis (Bd) infection, which is well known to infect keratinized structures such as the jaw sheaths and tooth rows in tadpoles ( Knapp & Morgan 2006; Carvalho et al. 2017). Furthermore, the pathogen is widely distributed in this region of the Serra do Mar, in the Atlantic Forest biome, and there are records of tadpoles and adults of different species of anurans infected by the pathogen ( Lambertini et al. 2021; Ruggeri et al. 2020).

Understanding the morphology and natural history of tadpoles is essential for conserving the diversity of anurans, and significant advancements have been made in recent decades ( Provete et al. 2013). The true diversity of the Proceratophrys genus is still being revealed, and the use of integrative taxonomic approaches can shed light on understanding the evolutionary history and diversification in the group ( Dias et al. 2013b). Therefore, data from natural history, advertising calls and larval morphology are valuable lines of investigation that can help understand the species diversity within this group.

Figures

FIGURE 1. Tadpole of Proceratophrys belzebul. (A) lateral view of tadpole in life and (B) dorsal view of body; (C) detail of the rostral region showing the nostrils (arrow); (D) detail of the spiracle (arrow); (E) detail of the oral disc.